Maturity and Fecundity of Lizardfish (Saurida undosquamis Richardson, 1848) in skenderun Bay (Eastern Mediterranean)

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1 Turk J Zool 27 (23) TÜB TAK Maturity and Fecundity of Lizardfish (Saurida undosquamis Richardson, 1848) in skenderun Bay (Eastern Mediterranean) Ali fimen Çanakkale Onsekiz Mart University, Faculty of Fisheries, P.O. Box 56, 171, Çanakkale - TURKEY alismen@yahoo.com Received: Abstract: The spawning season, size and age at first sexual maturity, and fecundity of the commercially important lizardfish (Saurida undosquamis) were studied on the basis of 62 specimens from skenderun Bay in the eastern Mediterranean. Lizardfishes had ripe gonads all around the year. The monthly gonadosomatic index values and the frequency of ripe gonads indicated that the spawning of this species occurred mainly in two seasons (May-July and September-November). Males attained first sexual maturity at a total length of about 16 cm and females at about 16.5 cm. Fecundity-length relationships estimated between 1999 and 2 were log F = log L (r =.76), log F = log L (r =.86), respectively. In 1999 and 2, fecundityage relationships were estimated as log F = log A (r =.8), log F = log A (r =.82), respectively. No annual variation in fecundity was apparent for the study period. Key Words: skenderun Bay, Lizardfish (Saurida undosquamis), First Sexual Maturity, Fecundity skenderun Körfezi (Do u Akdeniz) Iskarmoz Bal n n (Saurida undosquamis Richardson, 1848) Efleysel Olgunlu u ve Yumurta Verimi Özet: Do u Akdeniz de skenderun Körfezi nin ticari önemi yüksek bal klar ndan biri olan Iskarmoz bal n n (Saurida undosquamis) yumurtlama mevsimi, ilk efleysel olgunluk boyu, yafl ve yumurta verimi (fekondite) örneklenen 62 bireyde çal fl lm flt r. Iskarmozlar n tüm y l boyunca olgun gonadlara sahip oldu u saptanm flt r. Ayl k gonadosomatik indeks (GSI) de erleri ve olgun gonad frekanslar, bu türün esas olarak iki dönemde (May s-temmuz ve Eylül-Kas m) yumurtlad n göstermifltir. Erkekler ilk efleysel olgunlu a yaklafl k 16 cm; difliler ise 16.5 cm toplam boyda ulaflm fllard r ve 2 y llar nda yumurta verimi-boy iliflkisi s ras yla; log F = log L (r =.76), log F = log L (r =.86) olarak saptanm flt r ve 2 y l nda yumurta verimi-yafl iliflkisi s ras yla; log F = log A (r =.8), log F = log A (r =.82) olarak hesaplanm flt r. Bu çal flma süresinde yumurta veriminde y llara göre bir de iflim görülmemifltir. Anahtar Sözcükler: skenderun Körfezi, Iskarmoz Bal (Saurida undosquamis), lk Efleysel Olgunluk, Yumurta Verimi Introduction The lizardfish (Saurida undosquamis) is a Lessepsian migrant species that penetrated into the Mediterranean Sea from the Indo-West Pacific through the Suez Canal (Ben-Tuvia, 1966; Gücü et al., 1994; Mater et al., 1995). This species invaded the Levant Basin, and established a population of considerable commercial importance. The first report about lizardfish in Turkish seas was by Kosswig (1951). This is a demersal species, found over mostly sandy or muddy bottoms of coastal waters as deep as 2 m. It is reported that the maximum size of this fish is about 5 cm; however, in catches the common size range is between 2 and 3 cm (Bauchot, 1987). In the eastern Mediterranean (North Levantine Basin), S. undosquamis is among the most common species caught in the trawl fishery, accounting for 17-18% annually (Bingel et al., 1993). Comprehensive studies on the biology and ecology of this species are scarce. In the eastern Mediterranean, except for a few studies on its reproduction (Bingel, 1988a) and food intake (Bingel and Avflar, 1988a,b; Bingel, 1988b), most of the work deals with its distribution (Ben-Yami and Glaser, 1974; Golani, 1993) and general biology (Golani, 199; Torcu, 1995). Gücü and Bingel (1994) reported most Lessepsian species to be found on the continental shelf of the Northeastern Levantine Basin. Gücü et al. (1994) and Baflusta (1997) studied the distribution of Red Sea species along the Turkish coast. Payza (1983) investigated the enzyme system in three species (S. undosquamis, M. barbatus and 231

2 Maturity and Fecundity of Lizardfish (Saurida undosquamis Richardson, 1848) in skenderun Bay (Eastern Mediterranean) U. moluccensis) of the eastern Mediterranean for use in a biochemical genetic method of stock differentiation. Avflar et al. (199) studied the morphometric separation of lizardfish stocks in the Gulf of Mersin using the Mahalanobis distance function. Türeli and Erdem (1997), and Torcu (1995) reported observations on its age, growth, food and reproduction in skenderun Bay. This paper presents results from spawning time, length and age at first maturity and fecundity studies on lizardfish in skenderun Bay and the eastern Mediterranean in relation to length and age, and compares the fecunditylength relationship in different years. Materials and Methods Six hundred two lizardfish specimens were collected by monthly sampling using the R/V Mustafa Kemal-1 from May 1999 to June 2 in skenderun Bay. The bottom trawling operations were carried out in the areas circled in Figure 1 only during the daytime at depths ranging from 1 to 5 m. The trawl was equipped with a 18-mm mesh size net at the cod-end. Hauling lasted about 2.5 h at a towing speed of 1.5 kn. Due to adverse weather conditions, it was not possible to collect specimens in March or April E T U R K E Y Dörtyol 36.5 N Yumurtal k skenderun Bay Karatafl skenderun Arsuz N 36.2 N Ak nc Burnu Mediterranean Samanda 2 km Figure 1. Location of the sampling stations in skenderun Bay (O: sampling station). 232

3 A. fimen Samples were kept in ice boxes until transfer from the boat to the laboratory. Total length was measured to the nearest millimeter and body and gonad weights to the nearest gram in the laboratory. Age was determined from rings in the sagittal otoliths. Otoliths removed from the fish were cleaned with water and alcohol, and then stored dry in paper envelopes. The otoliths were sectioned across the center of the nucleus, using a scalpel, and the section or surface of otoliths was polished in order to make it much easier to read. The otoliths (the number of opaque and hyaline zones) were examined in glycerin under a stereozoom microscope illuminated from above (Holden and Raitt, 1974). For the age determinations, 1 January was used as the date of birth (Holden and Raitt, 1974; Bingel, 22). The length distributions of lizardfish and the back-calculation method in otolith readings were used to distinguish true annual zones from secondary or false zones. The degree of sexual maturity of each specimen was determined by inspection of the gonads in fresh individuals. The stages of maturation were classified according to Holden and Raitt s (1974) scale. The typical appearance of the gonad at each maturity stage is described below. Stage I (immature): Gonads are very small. Ovaries are pinkish translucent. Testis is whitish. Stage II (maturing and recovering spent): Gonads are small, dully transparent and pinkish-whitish. Stage III (ripening): Gonads are enlarged. Ovary is pinkish-yellow with granular appearance. Testis is whitish to creamy. There are no transparent ova. Stage IV (ripe): Gonads are considerably enlarged. Ovary is orange-pink with conspicuous superficial blood vessels and is large and transparent. Ripe ova are visible. Testis is whitish-creamy, soft. Stage V (spent): Gonads are shortened, walls loose, flabby, empty, dark red with traces of sperm or ova. The gonadosomatic index (GSI) was calculated by monthly period with the equation given below: GSI = (gonad weight/fish weight without gonad)*1 The mean lengths (cm) at 5% maturity from the percentages of mature lizardfish were calculated with 1- cm length intervals. Ovaries were cut longitudinally and stored in Gilson s fluid to dissolve the connective tissue. The egg numbers were estimated using the gravimetric method described by Bagenal (1978). The subsamples for counting were taken from anterior, middle and posterior parts of the ovary. All samples was counted three times under a stereozoom microscope and the mean value was calculated. The fecundity was estimated by multiplying the mean value with the factor G/g, where (G) is the gonad weight and (g) is the subsample weight. In all species the fecundity appears to be related to the length of the fish by an equation of the type F = al b. Therefore, the fecundity estimates were converted to a linear form using log-log (base 1) transformations, and the data were analyzed by least squares regression. Analysis of covariance (Rohlf, 1986) was used to test the significance of the differences between regression coefficients. Results The sex ratios of lizardfish for the study period in skenderun Bay were 38.8% for males and 61.2% for females. Changes in maturity and GSI Gonads classified by their macroscopic appearance are given in Table 1. The ripe fish (stage IV) in samples taken at monthly intervals showed that the spawning season extends over 12 months of the year. The intensity of spawning in each month throughout the spawning period Table 1. Number of fish in each maturity stage between May 1999 and June 2. Months Maturity Stages N I II III IV V May June July August September October November December January February March April May June

4 Maturity and Fecundity of Lizardfish (Saurida undosquamis Richardson, 1848) in skenderun Bay (Eastern Mediterranean) showed that most fish spawn during two main seasons (May-July and September-November). Monthly changes in the GSI revealed that gonad development was remarkably high between May and June (Figure 2). After June, the GSI showed a sharp decline and then increased slowly again between September and October. These periods coincide with the two main spawning periods. GSI May Figure 2. Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Months The monthly changes in the gonadosomatic index (GSI) of lizardfish. Length and age at first sexual maturity The transition from immaturity to maturity usually occurs over a range of lengths and is not abrupt, and this is reflected by the data presented in Table 2. Males attain sexual maturity at a total total length of about 16 cm and females at about 16.5 cm (Figure 3). These lengths at first sexual maturity coincide with age group I. Males have an average total length of 13.4 cm (1-16 cm) in age group I, and 17.7 cm (14-19 cm) in age group II. Females have an average total length of 14.6 cm (9-17 cm) in age group I, and 19.6 cm (16-22 cm) in age group II. Mature fish below 11 cm for males and 13 cm for females were not recorded. All males (1%) above 21 cm in total length and all females (1%) above 22 cm in total length were mature (Table 2). Fecundity related to fish length For skenderun Bay, the analysis of data for 1999 and 2 indicated that the fecundity of S. undosquamis is related to length by the relationships Table 2. Percentage distribution of ripe gonads of lizardfish in relation to the length groups (F: females, M: males). Mean (Three Length N Immature Ripe (n) Ripe (%) Running Averages) (cm) F M F M F M F M F M

5 A. fimen 1 9 Male Total length (cm) Female Total length (cm) % ripe % ripe Figure 3. The mean lengths at 5% maturity of lizardfish in each sex. Fecundity Fecundity Figure 4. F=aL n= Total length (cm) F=aL 3.49 n=35 (A) (B) Total length (cm) Relationships between fecundity and total length of lizardfish from skenderun Bay for 1999 (A) and 2 (B). log F = log L (1999) log F = log L (2) where (F) is fecundity (number of eggs) and (L) is fish length (cm). Plots of fecundity-length data and an arithmetic representation of the relationship are shown in Figure 4. In all cases the correlation coefficients (for 1999 r =.76, and for 2 r =.86) are significantly different from zero (P <.1) (Table 3). Analysis of covariance of the fecundity-length data for skenderun Bay between 1999 and 2 indicated that there are no significances between the regression coefficients (rate of egg production) (P >.1). Fecundity related to fish age The fecundity-age relationship for skenderun Bay in 1999 and 2 is indicated by the expressions log F = log A (1999) log F = log A (2) where (A) is fish age (years). Plots of the data and the arithmetic representation of the equations are shown in Figure 5. The correlation coefficients (for 1999 r =.8, and for 2 r =.82) for all relationships are significantly different from zero (P <.1) (Table 3). Analysis of covariance of the 1999 and 2 fecundity-age data for skenderun Bay indicated that there are no significant differences between the regression coefficients (P >.1). Discussion The ripe fish (stage IV) in samples taken at monthly intervals in skenderun Bay showed that the spawning season extends over 12 months of the year. The intensity of spawning in each month (Table 1) and the GSI results revealed that most fish spawn during two main seasons (May-July and September-November). These results are similar to those determined in other studies on lizardfish in this area (Ben-Tuvia, 1966; Bingel, 1988a; Ben-Yami and Glaser, 1974; Torcu, 1995; Arakawa, 1993; TÜGM, 1993). Ben-Tuvia (1966) reported that Red Sea species in the eastern Mediterranenan reproduce in late spring and summer. It is likely that the same species in the southern Red Sea reproduce throughout the year. Ben- Yami and Glaser (1974) stated that ripe, nearly ripe, and partly spent females occur in catches almost all year around, although the former author indicated that the greater proportion of nearly ripe females occurs in the 235

6 Maturity and Fecundity of Lizardfish (Saurida undosquamis Richardson, 1848) in skenderun Bay (Eastern Mediterranean) Fecundity Fecundity Figure 5. F=aA n= Age F=aA.925 n= Age early summer. They stated that lizardfish may spawn over a prolonged season, while the survival of its fry may be confined to a much shorter period controlled by favorable seasonal conditions. Bingel (1988a) studied the spawning of S. undosquamis in the Tırtar and Göksu regions along the Turkish eastern Mediterranean coast, and noted that the measured ovary weights show two clear and distinct spawning seasons (June-July and September-October). He also stated that there are probably early, intermediate and late spawners of the two main spawning periods and based on eventually (A) (B) Relationships between fecundity and age of lizardfish from skenderun Bay for 1999 (A) and 2 (B) unfavorable conditions. Arakawa (1993) and the TÜGM (1993) studied the resources of demersal fishes by seasonal sampling off the Turkish Mediterranean coast and stated that lizardfish may spawn throughout the year, with maxima in spring (April-July) and fall (September-November). Torcu (1995) reported that GSI results revealed that reproduction in the eastern Mediterranean Sea occurred after August when the GSI reached its highest level. The spawning season and fecundity of the same species have been reported to vary from one geographical area to another. This may result from differences in growth rates, and seasonal, geographical and ecological conditions. Bauchot (1987) stated that lizardfish spawn from April to May off Japan; and in addition to this, Sanders and Morgan (1989) reported that in the Suez Canal, lizardfish reproduce partly in April, May and June, being fully active in other months. The sex ratios for the study period were 38.8% for males and 61.2% for females in skenderun Bay. This result agrees with the results of other studies performed in the eastern Mediterranean. Based on the data given by Torcu (1995), the sex ratios of lizardfish can be calculated as.39% for males and.61% for females at Fethiye and Mersin on the Mediterranean coast of Turkey. Bingel (1988a) noted that the sex ratios were 37.95% for males and 62.5% for females at Göksu and 34.83% for males and 65.17% for females at Tırtar. The TÜGM (1993) stated that females predominate over males in all seasons and the sex ratio was 1.67 in fall and in other seasons. The total length and age at 5% maturity (first maturity) for males and females in this study were 16 cm Table 3. Regression constants and significance tests in correlations of fecundity with length and age for lizardfish from skenderun Bay in 1999 and 2. Years No. of fish Slope Intercept r (b) (log a) Fecundity-length ** ** Fecundity-age ** ** ** Significant, P <.1 236

7 A. fimen (age group I) and 16.5 cm (age group I), respectively. This result agrees with other studies; e.g., Arakawa (1993) and the TÜGM (1993) reported that lizardfish along the Turkish eastern Mediterranenan coast attained sexual maturity at age I. No data are available for the length at first sexual maturity. However, the TÜGM (1993) stated that the mean fork lengths in age group I for males and females are 2.6 cm and 23.4 cm in spring, 16.7 cm and 17.2 cm in summer, 16.8 cm and 17.3 cm in fall, and 15.1 and 2.5 cm in winter, respectively. Fecundity-length relationships estimated between 1999 and 2 were log F = log L (r =.76) and log F = log L (r =.86), respectively. In 1999 and 2, fecundity-age relationships were estimated as log F = log A (r =.8) and log F = log A (r =.82), respectively. Since no data are available on the fecundity-length and fecundity-age relationships, the results could not be compared with them. There is only one observation on the number of eggs produced in the eastern Mediterranean Sea. Torcu (1995) found that the fecundity of lizardfish, which were g in weight, is 14,226-65,833 in Mersin Bay. Annual fluctuations in the fecundity of lizardfish were not apparent in this study. Oosthuizen and Daan (1974), Buzeta and Waiwood (1982), Bowering (198) and flmen (1995) compared the fecundity of some teleost fishes like cod and whiting in relation to years and they were also unable to detect any significant change. However, such variation has been reported in many studies. Bagenal (1963) attributed annual fluctuations in the fecundity of witch flounder (Glyptocephalus cynoglossus) to changes in fishing intensity, which in turn affected fecundity through variations in the food supply. He also concluded that the variation in fecundity was not related to changes in hydrographic conditions. Pinhorn (1984) found some annual variations in the fecundity of Newfoundland cod. He attributed the observed variation to less feeding and a slower digestion rate because of changing water temperature. Acknowledgments This work was sponsored under project- 99E-371 by Mustafa Kemal University Research Fund. I would like to acknowledge the help of Sefa A. Demirhan and Pınar flmen in sample collection. I also thank the crews of R/V Mustafa Kemal-1 for their valuable help. References Arakawa, I Survey Report of Demersal Fishery Resources and Data Collection in Turkey. Group Work, Sanyo, Techno. Uni., Tokyo, Japan, (in Turkish), pp Avflar, D., Bingel, F., and Ünsal, M Applications of Mahalanobis Distance Function for the Morphometric Separation of Lizardfish (S. undosquamis) Stocks in the Gulf of Mersin. METU Journal of Pure and Applied Sciences, 2: Bagenal, T.H The fecundity of witches in the Firth of Clyde. J. Mar. Biol. Assoc. UK, 43: Bagenal, T.B Fecundity. In: T.B. Bagenal (ed.), Methods for assessment of fish production in fresh waters. IBP Handbook No: 3, Blackwell Scientific, London, pp Baflusta, N Pelagic and demercial fishes in Iskenderun Bay. PhD thesis, C.U. Science Institute, Adana, 22 pp. Bauchot, M.-L Poissons osseux. In W. Fischer, M.L. Bauchot and M. Schneider (eds.) Fiches FAO d identification pour les besoins de la peche (rev. 1). Mediterranee et mer Noire. Zone de peche 37. Vol II. Commission des Communautes Europeennes and FAO, Rome, pp Ben-Yami M. and Glaser, T The invasion of S. undosquamis into the Levant Basin an example of biological effect of interoceanic canals. Fishery Bulletin, 72: Ben-Tuvia, A Red Sea fishes recently found in the Mediterranean. Copeia, 2: Bingel, F. 1988a. A note on the spawning of Saurida undosquamis in the northern Cilician Basin. Turkish coast. Rapp. Comm. Int. Mer. Medit., 31, p. 27. Bingel, F. 1988b. Prey size of Saurida undosquamis in the Northern Cilician Basin (Eastern Mediterranean). Rapp. Comm. Int. Mer. Medit., 31, p Bingel, F. 22. Balık Populasyonlarının ncelenmesi. Yayın No: 26, Baki Kitapevi, çel, 44 s. Bingel, F. and Avflar, D. 1988a. Food items of Saurida undosquamis in the Northern Cilician Basin (Eastern Mediterranean). Rapp. Comm. Int. Mer. Medit., 31, p Bingel, F. and Avflar, D. 1988b. Time series of the stomach fillings of Saurida undosquamis in the Northern Cilician Basin (Eastern Mediterranean). Rapp. Comm. Int. Mer. Medit., 31, p

8 Maturity and Fecundity of Lizardfish (Saurida undosquamis Richardson, 1848) in skenderun Bay (Eastern Mediterranean) Bingel, F., Özsoy, E. and Ünluata, Ü A review of the state of the fisheries and the environment of the Northeastern Mediterranean (Northern Levantine Basin). Studies and Reviews, General Fisheries Council for the Mediterranenan. No: 65, Rome, FAO, 74 pp. Bowering, W.R Fecundity of Greenland Halibut, Reinhardtius hippoglossoides, from Southern Labrador and Southeastern Gulf of St. Lawrence. J. Northwest. Atl. Fish. Sci., 1: Buzeta, M.-I and Waiwood, K.G Fecundity of Atlantic cod (Gadus morhua) in the Southwestern Gulf of St. Lawrence. Can Tech. Rep. Fish. Aquat. Sci., 111: 6 pp. Golani, D Environmentally induced meristic changes in Lessepsian fish migrants, a comparison of source and colonizing populations. Bull. l Instıtut Ocean. Monaco (special issue) 7: Golani, D Trophic adaptations of Red Sea fishes to the eastern Mediterranean environment review and new data. Isr. J. Zoo., 39: Gücü, A.C. and Bingel, F Trawlable species assemblages on the continental shelf of the North eastern Levant Sea (Mediterranean) with an emphasis on Lessepsian migration. Acta Adriatica, 35: Gücü, A.C., Bingel, F., Avflar, D. and Uysal, N Distribution and occurrence of Red Sea fish at the Turkish Mediterranean coastnorthern Cilician basin. Acta Adriatica, 34: Holden, M.J. and Raitt, D.F.S Manual of fisheries science. Part: 2-Methods of resource investigation and their application. FAO Fish. Tech. Rap. (115): Rev. 1, 214 pp. flmen, A Fecundity of whiting, Merlangius merlangus euxinus, on the Turkish Black Sea coast. Fisheries Research, 22: Kosswig, C Contributions to the knowledge of the zoogeographical situation in the near and Middle East. Experentia, 7: Mater, S., To ulga, M. and Kaya, M Distribution of Lessepsian fish species at the Turkish Sea. II. National Ecology and Enviroment Congress, September 1995, (in Turkish), pp Oosthuizen, E. and Daan, N Egg fecundity and maturity of North Sea cod (Gadus morhua). Neth. J. Sea. Res., 8: Payza, K Biochemical genetic study of three fish species of the eastern Mediterranean. MS Thesis. Institute of Marine Sciences, METU, 21pp. Pinhorn, A.T Temporal and spatial variation in fecundity of Atlantic cod (Gadus morhua) in Newfoundland waters. J. Northwest. Atl. Fish. Sci. 5: Rohlf, F.J Biom. A package of statistical programs to accompany the text Biometry. State University of New York, 18 pp. Sanders, M.J. and Morgan, G.R Review of the fisheries resources of the Red Sea and Gulf of Aden. FAO Fish. Tech. Rep. (34): 138 pp. Tarımsal Üretim ve Gelifltirme Müdürlü ü (TÜGM), Survey Report of Demersal Fishery Resources in Marmara, Aegean and Mediterranean. T.C. TKIB, Tarımsal Üretim ve Gelifltirme Mudurlugu- JICA, (in Turkish), 579 pp. Torcu, H Studies on Biology and Ecology of Indo-Pacific fishes Goatfish (Upeneus moluccensis) and Lizardfish (Saurida undosquamis) found in the Mediterranean and South Aegean Sea coasts. Selçuk Uni. Science Inst. PhD Thesis, Konya, (in Turkish), 168 pp. Türeli, C. and Erdem, U The growth performance of Red Mullet (M. barbatus) and Brushtooth Lizardfish (S. undosquamis) from the coastal region of Adana province ( skenderun Bay, Turkey). Tr. J. of Zoology, 21:

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